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IJBPAS, January, 2016, 5(1): 362-375 ISSN: 2277–4998
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IJBPAS, January 2016, 5(1)
SEASONAL HISTOMORPHOMETRIC STUDIES ON THE EPIDIDYMAL DUCT
OF THE ONE-HUMPED CAMEL (CAMELUS DROMEDARIUS)
MOHAMED EL-SAKHAWY1, MAMDOUHEL-SHAMMAA2, SHAYMAA HUSSEIN3*,
ABDEL-ALEEMEL-SABAA, A4AND YAHYA AHMED5
1, 2, 3, 4: Department of Cytology and Histology, Faculty of Veterinary Medicine, Cairo. University, Egypt
5: Department of Veterinary Anatomy, Mosul University, Iraq5 E Mail: [email protected]
ABSTRACT
This investigation was carried on right and left epididymis of 76 sexually mature (6-7 years)
apparently healthy, one humped camel ( Sudanese breed ), which collected directly after
slaughtering from Kerdasa slaughter house, Giza , Egypt all over the year from December
2011 till November 2012. The epididymis was composed of the efferent ductules and the
epididymal duct. The epididymal duct was divided into initial, middle and terminal segments.
The middle segment was subdivided into proximal, intermediate and distal parts. The
terminal segment was further subdivided into proximal and distal parts. Samples from
different regions were processed histologically. Paraffin sections 5-6 µmthick were stained
with H&E, Van Gieson's, Masson's trichromeand PASstains were used for
histomorphometrical study. The epididymal duct showed significant seasonal changes in the
total diameter, epithelial height, length of stereocilia, luminal diameter, thickness of
peritubular muscular coat and the cellular distribution. The values of these elements were
increase during spring season in comparison with other seasons. The results were analyzed
statistically.The epididymal duct was lined by a pseudostratified columnar epithelium. The
epididymal epithelium was composed of five cell types: principal, basal, apical, dark and halo
cells. Abundant apical like protrusions, numerous cytoplasmic vacuoles and PAS positive
granules characterizing the principal cells in spring season. In conclusion the spring season is
the breeding season in camel in Egypt.
Keywords: Seasonal changes, epididymis, camel, histomorphometry
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INTRODUCTION
Camel is described as a seasonal breeder
(Al Eknah, 2000 and Maraiet al.,2009) or it
may maintain their reproductive capacity
throughout the year (Zayedet al., 1995).
The seasonal breeding behavior of the male
camel is referred to as rut (Khanet
al.,2003).The onset of breading season of
male camel is markedly divergent in Egypt.
The rutting season has been reported to
occur at December uptill March (Ebada,
1994), while according to Abd El-maksoud
(2010) the rutting season occurs during
spring. The excurrent duct system of the
testis includes the efferent ductules, the
ductus epididymidis and the ductus
deferens (Roberts, 2010). The epididymis
consists of highly convoluted duct that
links the efferent ductules to the vas
deferens (Turner et al.,2003).Like other
economically valuable animals, studying
the morphology of the camel reproductive
organs is essential to improving and
exploiting their reproductive activity.
Detailed description of the structure of the
epididymal duct and their morphometry in
the dromedary during breeding and non-
breeding seasons has been quite few (Abd
El-maksoud, 2010). In addition, data on the
stage of seasonal changes in camel are
quite divergent. In view of this, the aim of
this study is to elucidate more light and
some details on the histomorphometrical
features of the epididymal duct of the one
humped camel during different seasons.
MATERIAL AND METHODS
Right and left epididymis of 76 sexually
mature (6-7 years) apparently healthy, one
humped camel ( Sudanese breed ) were
collected directly after slaughtering from
Kerdasa slaughter house, Giza , Egypt all
over the year from December 2011 till
November 2012.
Anatomically, the epididymal duct was
consisted of three regions; head (caput),
body (corpus) and tail (cauda).
Histologically and histomorphometrically,
the epididymis in the present investigation
was subdivided into 7 parts. The head
(caput) was subdivided into two parts,
ascending first part of the head and initial
part of epididymal duct. The middle
segment (corpus) was further subdivided
into proximal, intermediate and distal parts
and finally the terminal segment (cauda)
was composed of proximal and distal parts
(Fig.1).
The present study included the following
lines:
1- General histological study:
The obtained segments were fixed in
buffered 10 % formalin of (pH 7.0) and
Bouin′s fluid for 24 hours. Fixed specimens
were dehydrated, cleared and embedded in
paraffin wax. Step serial sections of 5-6 µm
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IJBPAS, January 2016, 5(1)
thick were obtained and stained with:Harris
hematoxyline and eosin (H&E), Van
Gieson's stain, Masson's trichrome
stain,Periodic acid Schiff technique (PAS).
The aformentioned methods were used as
outlined by Drury and Wallingtion (1980).
2– Histomorphometrical and statistical
analysis:
Sections stained with H&E, Van Gieson's,
Masson's trichromeand PAS stains were
used for histomorphometrical study.
Approximately 10 tubular cross sections
from each epididymal parts were measured
by high power lens (X 40). A computerized
microscopic image analyzer attached for
full HD microscopic camera (Leica
Microsystems, Germany) was used to
determine the histomorphometric
parametes. The data were tested firstly for
normal distribution using Normality test.
Normal distributed data were compared by
ANOVA (One-Way Analysis of Variance).
Significant differences were determined by
Duncan’s Multiple Range Test. The data
sets, that had not fulfilled the assumption of
normal distribution, were analyzed using
Kruskal- Wallis One Way Analysis of
Variance on Ranks. Significant differences
were determined by Dunn’s Test. All
statistical analyses were performed by
SigmaStat (Jandel scientific software
V3.1).
Table 1: Total diameter (Mean±SE) of different segments of the camel epididymal duct in different seasons
Segments Total diameter (µm)
Winter (January) Spring (may)
Summer (July )
Autumn (October)
Initial segment (IS) 156.851±4.102 a,b
163.498±4.649 a
139.31±4.183 b
150.219±5.054 a,b
Middle segment (MS)
Proximal part (P)
97.075±6.639 a
152.66±5.062 b
121.859±6.966 c
135.39±4.02 b,c
Intermediate part (I)
115.19±9.238 a
133.078±6.387 a
131.654±1.147 a
125.669±5.959 a
Distal part (D)
111.383±3.601 a
169.428±5.981 b
153.516±5.772 b,c
143.443±4.335 c
Terminal segment
(TS)
Proximal part (P)
168.33±3.263 a,c
208.316±9.284
187.385±18.487 c
163.104±7.396 a
Distal part (D)
182.421±8.001 a
246.311±13.871 b
217.951±5.759 c
232.325±6.216 b,c
a-c Values with a different superscript within rows were significantly different (P<0.05)
Table 2: Epithelial height (Mean±SE) of different segments of the camel epididymal duct in different seasons Segments Epithelial height (µm)
Winter (January) Spring (may) Summer (July ) Autumn (October) Initial segment (IS) 32.582±0.942
b 42.634±1.558
a 34.569±1.663
b 32.094±1.206
b Middle segment
(M) Proximal
part (P) 12.569±1.201
b 27.208±1.526
a 25.743±3.16
a 24.427±2.043
a Intermediate part
(I) 20.047±2.502
b 29.267±0.637
a 22.374±0.841
b 21.056±1.872
b Distal
part (D) 17.673±1.502
b 26.809±1.068
a 18.143±0.411
b 19.149±1.861
b Terminal segment
(TS)
Proximal part (P)
11.286±0.897 c
31.11±1.306 a
24.501±1.17 b
22.218±1.659 b
Distal part (D)
11.268±0.457 b
19.115±1.045 a
17.143±0.322 a,c
13.418±0.947 b,c
a-c Values with a different superscript within rows were significantly different (P<0.05)
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Table 3: Length of stereocilia (Mean±SE) of different segments of the camel epididymal duct
Segments Length of stereocilia (µm)
Winter (January) Spring (may)
Summer (July )
Autumn (October)
Initial segment (IS) 3.329±0.334 A
4.16±0.503 A
3.346±0.598 a
3.972±0.532 a
Middle segment
(MS)
Proximal Part (P)
2.437±0.687 A
6.591±0.189 B
3.609±0.289 c
5.149±0.453 d
Intermediate part (I)
2.51±0.124 b
3.774±0.585 a
3.767±0.319 a
1.609±0.168 b
Distal part (D)
1.579±0.216 a
2.14±0.0374 a
2.049±0.285 a
1.151±0.0236 a
Terminal segment
(TS)
Proximal part (P)
1.803±0.141 a
1.915±0.129 a
1.242±0.232 a
1.888±0.174 a
Distal part (D)
1.325±0.0851 a
1.964±0.248 a
1.406±0.178 a
0.923±0.0494 a
a-d Values with a different superscript within rows were significantly different (P<0.05).
Table 4: Luminal diameter (Mean±SE) of different segments of the camel epididymal duct in different seasons
Segments Luminal diameter (µm)
Winter (January)
Spring (may)
Summer (July )
Autumn (October)
Initial segment (IS) 76.528±6.347 b
98.832±4.949 a
83.774±3.657 a,b
80.629±9.321 a,b
Middle segment
(MS)
Proximal part (P)
71.251±8.015 b,c
98.466±4.92 a
71.026±2.984 b,c
84.668±4.145 a,c
Intermediate part (I)
76.481±4.729 a
88.82±5.369 a
75.273±1.558 a
84.79±9.212 a
Distal part (D)
75.83±3.922 a
120.507±5.936 b
117.568±6.552 b
104.939±1.7 b
Terminal segment
(TS)
Proximal part (P)
145.91±3.035 a,c
164.503±10.372 a
139.586±20.754 b,c
100.901±6.057 b
Distal part (D)
162.501±7.978 a
206.266±7.312 b
184.759±6.255 a,b
201.229±8.58 b
a-c Values with a different superscript within rows were significantly different (P<0.05)
Table 5: Thickness of muscular coat (Mean±SE) of different segments of the camel epididymal duct in different seasons
Segments
Thickness of muscular coat (µm) Winter (January) Spring
(may) Summer (July )
Autumn (October)
Initial segment (IS) 8.616±1.151 a
12.174±1.315 b
10.826±0.524 a,b
10.303±0.754 a,b
Middle segment (MS)
Proximal part (P)
7.087±1.131 b,c
10.581±1.245 a
7.853±0.602 b,c
8.386±0.954 a,c
Intermediate part (I)
7.168±0.508 b
10.668±0.764 a
7.268±0.523 b
8.846±0.301 b
Distal part (D)
6.788±0.653 b,c
9.747±0.378 a
6.682±0.784 b,c
8.167±0.259 a,c
Terminal segment (TS)
Proximal part (P)
15.162±0.921 b
21.638±0.732 a
14.336±1.381 b
20.285±0.734 a
Distal part (D)
16.446±0.809 b
24.19±1.897 a
22.244±0.234 a
18.403±0.367 b
a-c Values with a different superscript within rows were significantly different (P<0.05).
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Fig. (1). Schematic drawing of the right testis and epididymis of camel. The head, body and tail had been dissected from the upper
pole of the testis and stretched to show the different segment of the epididymis from which the specimens were obtained. 1-Ascending first region of the head, 2- Initial segment ( IS), 3-Proximal part of the middle segment (MS-P) ,4-Intermediate part of the middle segment (MS-I) ,5-Distal part of the middle segment (MS-D), 6-Proximal part of the terminal segment (TS-P), 7-Distal
part of the terminal segment (TS-D).
Fig. (2). A photomicrograph of a section at the level of the initial segment of camel epididymal duct during spring showing:
Principal cell (P) and its PAS positive supra and infranuclear cytoplasmis granules (arrow heads), Halo cell (H), apical cell (A) and PAS positive stereocilia (arrow) PAS X 1000
Fig. (3). A photomicrograph of a section at the level of the distal part of terminal segment of camel epididymal duct during spring showing: Principal cell (P) with its oval nuclei in the lower third, numerous vacuoles and PAS positive granules (star) in the apical
part, basal cell with its large PAS positive globule (arrow) and intense PAS positive stereocilia (arrow head). PAS X 1000
3
1
2
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Fig. (4). A photomicrograph of a section at the level of the initial segment of camel epididymal duct during summer season showing:
Principal cells (P) with their condensed irregularly oval heterochromatic nuclei. PAS X 1000
Fig. (5). A photomicrograph of a section at the level of the distal part of middle segment of camel epididymal duct during spring
showing: Principal cells (P) with their PAS positive granules (arrow head) and apical like protrusions. Basal cell with its PAS positive globule (double arrows); PAS X 1000
Fig. (6). A photomicrograph of a section at the level of the distal part of middle segment of camel epididymal duct during autumn
season showing: Numerous dark cells (D); PAS X 1000 Fig. (7). A photomicrograph of a section at the level of the intermediate part of the middle segment of camel epididymal duct during
summer season showing: - Lumina (L) contained few spermatozoa H & E X 40
4
5
6 7
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Fig. (8). A photomicrograph of a section at the level of the initial segment of camel epididymal duct during spring showing:
Peritubular internal and external collagen fibers (arrows) and peritubular muscular coat (PMC) Van Gieson X 400 Fig. (9). A photomicrograph of a section at the level of the distal part of middle segment of camel epididymal duct during spring
showing: Increase in thickness of the peritubular muscular coat and aggregation of vacuolated basal cells (arrow) Masson's trichrome X 400
Fig. (10). A photomicrograph of a section at the level of the proximal part of terminal segment of camel epididymal duct during
spring showing: Peritubular fine collagen fibers (arrow head) and distribution of collagen fibers (arrow) among the thick peritubular smooth muscle fibers (stars) Van Gieson X 400
RESULTS AND DISSCUSION
The traditional macroscopic segmentation
of the epididymis into head, body and tail
was insufficient to reflect the structural-
functional relationship ofthis organ (Glover
and Nicander, 1971). Based on histological,
Histochemical and ultrastructural
characteristics, the epididymis of most
mammalian speciescould be subdivided
into several segments.The number and
distribution of these segments was species-
specific
(Wrobel, 1998). Furthermore, Glover and
Nicander (1971) stated that thenumber of
epididymal segments might vary within the
same species dependingupon the criteria of
classification. The number of epididymal
segments was eight in rabbit (Jones et al.,
1979) and buffalo (Abdouet al., 1985),
seven inguinea pig (Hoffer and Greenberg,
1978) and buffalo (Ebada, 2000), six
inbuffalo (Goyal and Dhingra, 1975), horse
(Lópezet al., 1989) and cat (Axneret
al.,1999), five in bull (Alkafafy, 2005) and
8 9
10
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goat (Goyal and Williams,1991), and four
in cat (Sanchez et al., 1998).
In camel and in consistence with Tingari
and Moniem (1979), Ebada(1994) and Abd
El-maksoud (2010) whom stated that, the
epididymis wassubdivided into initial,
middle and terminal segments, of which the
middlesegment was further subdivided into
proximal, intermediate and distal parts.The
current study did not support the previous
findings in camel, since theepididymis was
divided into initial, middle and terminal
segments. The middlesegment was further
subdivided into proximal, intermediate and
distal parts andthe terminal segment was
also subdivided into proximal and distal
parts. For these reasons, the epididymis of
camel in the present work was subdivided
into seven segments (with addition of
efferent ductules) (Fig. 1).
The epididymal duct was lined by a
pseudostratified columnar epithelium. The
epididymal epithelium was composed of
five cell types: principal, basal, apical,
darkand halo cells. These findings
simulated with former observations in the
camel (Tingari, 1989; Ebada, 1994 and Abd
El-maksoud, 2010).
The principal and basal cells were the most
frequent cell types throughout the whole
length of the epididymal duct. The
occurrence of the apical, dark and halo cells
was less numerous in comparisons with
those of principal and basal cells.
Macrophages and lymphocytes were found
scattered throughout the epididymal duct
and also present within the lumen.It was
possible that the macrophages along with
the lymphocytes might participate in the
induction of immune tolerance and thus
prevent the body from mounting immune
reaction against spermatozoa
(Marchlewicz, 2001). Also, the presence of
macrophages might be of some importance
in the process of sperm resorption.
Similar to findings of Abd El-maksoud
(2010) in camel, the present study showed
significant seasonal differences of the
epididymal duct expressed by total
diameter, epithelial height, length of
stereocilia, luminal diameter, thickness of
peritubular muscular coat and the cellular
distribution.
The total diameter showed significant
changes among different segments of the
epididymal duct in different seasons. It
decreased gradually from initial segment to
the intermediate part of the middle segment
then increased gradually in the distal part of
the middle segment until reaching the
maximum diameter in the distal part of the
terminal segment (Table 1). The above was
observed in all seasons.
On the other hand, the height of the
epithelium decreased toward the distal part
of the middle segment, and then the
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epithelial height increased in the proximal
part of the terminal segment followed by a
marked decrease in the distal part of such
segment (Table 2 and Figs. 2, 3).This
gradual decrease in the epithelial height
distal wards the epididymal duct might
mechanically facilitate passage of the
sperms toward the terminal segment (Abd
El-maksoud, 2010). Our observation
revealed that, the high epithelium in the
initial segment might however, indicated a
more absorptive power and secretory
activity of the epithelium in this segment.
In this respect, Crabo (1965) in bull had
been reported that, over 90% of the fluids
entering the epididymal duct was absorbed
in the head of the epididymis.
In the current study, the highest epididymal
epithelium was demonstrated in spring
season (Fig. 2) followed by summer (Fig.
4), autumn and winter. Singh and
Bharadwaj (1980) had been revealed that,
the epididymal epithelium increased in
height at December to March and Abd El-
maksoud (2010) recorded that, the slightly
low lining epithelium was identified in
spring season. The latter author illustrated
that the decreasing epithelial height in
spring season to higher activity, whereas
the high epithelium in other seasons was an
indication to low activity. This was due to
accumulation of secretion within the cells
of high epithelium.
The present investigation revealed that the
distribution and morphology of various
cells constituting the epididymal epithelium
showed significant seasonal changes. In all
seasons, the principle cells formed the
predominant cells throughout the whole
epididymal duct and displayed important
morphological changes from season to
another. In spring season, the nuclei of the
principal cells were vesicular oval with few
chromatin condensations mainly adherent
to the inner surface of the nuclear
membrane. These nuclei were displaced at
different levels in the cells (Fig. 2). The
nuclei of the principal cells were elongated
oval in winter season and condensed
irregular oval in summer (Fig. 4) and
autumn. The nuclei in the latter seasons
possessed numerous heterochromatin
patches and they were mostly arranged in
the basal parts of the cells. Similar to
findings of Abd El-maksoud (2010) in the
camel, the lightly stained oval nuclei in the
spring season indicating increased activity
of the principal cells comparing to the
darkly stained nuclei in other seasons; a
sign of the decreased activity.
In the same manner, our observations
showed that the abundant apical like
protrusions, the numerous cytoplasmic
vacuoles and PAS positive granules
characterizing the principal cells in spring
season (Fig. 5) were indication to increase
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absorptive and secretory activities
comparing with other seasons.In this
respect, López et al. (1989) had mentioned
that the epididymal epithelium synthesized
and secreted glycoproteins into the luminal
fluid, which was the carrier medium for
spermatozoa during the epididymal passage
and played a role in sperm maturation,
capacitation and fertilization activities.
Furthermore, Mandalet al.(2006) had found
protein factor termed as forward motility
stimulating protein (FMSF-1). This factor
was glycoprotein in nature and possessed a
physiological activator of sperm motility.
The principal cells function was secretion
and absorption. In addition to
glycoproteins, the principal cells secreted
proteins and enzymes such as phosphatases
and glycosidases which were essential in
the process of fertilization (Robaireet
al.,2006 and Samuelson, 2007).
In the present work, the basal cells did not
exhibited significant changes among the
different seasons. The dark cells in the
current study were never found in the distal
part of the terminal segment in spring
season, whereas in the other season
particularly in autumn, they were increased
in number distalwards of the epididymal
duct (Fig. 6). Abd El-maksoud (2010) in
camel mentioned that, the dark cells
increased in summer indicating decreased
activity after an activeperiod in spring.
The longest stereociliawere noticed in the
proximal part of the middlesegment, and
then decreased gradually distalwards till
they reached the lowest length in
theterminal segment (Table 3). These
findings were in accordance with the
precedingstudies in camel (Tingari and
Moniem, 1979) and contradict other studies
in the same animal (Ebada, 1994 and Abd
El-maksoud, 2010). The principal cells of
the equine caput and corpus epididymidis
were equipped with long stereocilia and
displayed morphological hallmarks of
absorption and digestive activities (López
et al., 1989). The stereocilia increased the
cell surface area facilitating the movement
of molecules into and out of the cell
(Junqueira and Carneiro, 2005).
In spring, the luminal diameter decreased
gradually toward the intermediatepart of
the middle segment, then increased
distalwards greatly. In spring, themaximum
luminal diameter was noticed in the distal
part of the terminal segment.Also,
maximum luminal diameter was reached in
all parts in spring season followed
byautumn, summer and winter (Table 4). In
spring, the lumina of the middleand
terminal segments were densely crowded
with sperms.
In summer, the middle segment of the
epididymal duct revealed few sperms
intheir lumen (Fig.7), while the lumen of
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the terminal segment showed no
sperms.During winter and autumn the
epididymal duct showed dispersed few
amount ofsperms within their lumen.
In the present study, the distal part of the
terminal segment was characterized by the
widest lumen and lowest epithelial height
comparing with other parts of the
epididymal duct. This made a place for
storage of sperms. Pineda (1989) and
Samuelson (2007) recorded that the
caudaepididymidis served as a reservoir for
storage of viable spermatozoa.
The highest thickness of the peritubular
muscular coat was apparent duringspring
season in all parts of the epididymal duct
(Table 5).Our results pointed that the
highest thickness of the peritubular
muscular coat was apparent during spring
season in all parts of the epididymal duct
comparing with other season. Furthermore,
there was an increase in the thickness of the
peritubular muscular coat till the distal part
of the middle segment (Figs. 8, 9), followed
by dramatic increase in the thickness of this
muscle in both parts of the terminal
segment(Fig. 10). In agreement with
findings of Abd El-maksoud (2010) in
spring season , the thickest muscular coat
observed in the terminal segment which
might be helpful for powerful ejaculation
(AlKafafy, 2005). In the present work, the
muscular coat consisted of circularly
arranged smooth muscle cells in the initial
and middle segments, whereas in the
terminal segment formed of abundant
circularly and obliquely arranged smooth
muscle fibers. According to Abd El-
maksoud (2010) in the camel, the obliquely
smooth muscle fibers in the terminal
segment increased in proportion and tended
to be longitudinally oriented. Furthermore,
the latter author mentioned that, the head
and body of the epididymis demonstrated
spontaneous rhythmic peristaltic
contractions that served to convey the
sperms along the duct. Fewer such
contractions were observed in the tail
region.
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